The Red Room received its name after red fabrics were used for the draperies, upholsteries and floor covering in the 1840s. Today the walls are covered in a red twill satin fabric with a gold design in the borders, and the furniture is upholstered in a silk of the same shade of red. The rug is a reproduction of a 19th century French Savonnerie carpet installed when First Lady Jacqueline Kennedy refurbished the room.

Beginning in 1809, First Lady Dolley Madison held gatherings every Wednesday in the Red Room to encourage socializing between members of opposing political parties. In 1933, First Lady Eleanor Roosevelt used the Red Room to host the first of many press conferences for women reporters who at that time were excluded from the President's press conferences.

The Red Room was also the site of the secret swearing-in of President Rutherford B. Hayes right after his hotly contested defeat of Samuel J. Tilden in the election of 1876. Inauguration fell on a Sunday that year. To avoid a possible coup, he took the oath of office in the Red Room and then again in public on March 5, 1877.